Abstract
Before fertilization, oocytes of most species undergo a long, natural arrest in metaphase. Before this, prometaphase I is also prolonged, due to late stable kinetochore-microtubule attachment. How oocytes stably maintain the dynamic spindle for hours during these periods is poorly understood. Here we report that the bipolar spindle changes its molecular architecture during the long prometaphase/metaphase I in Drosophila melanogaster oocytes. By generating transgenic flies expressing GFP-tagged spindle proteins, we found that 14 of 25 spindle proteins change their distribution in the bipolar spindle. Among them, microtubule cross-linking kinesins, MKlp1/Pavarotti and kinesin-5/Klp61F, accumulate to the spindle equator in late metaphase. We found that the late equator accumulation of MKlp1/Pavarotti is regulated by a mechanism distinct from that in mitosis. While MKlp1/Pavarotti contributes to the control of spindle length, kinesin-5/Klp61F is crucial for maintaining a bipolar spindle during metaphase I arrest. Our study provides novel insight into how oocytes maintain a bipolar spindle during metaphase arrest.
Highlights
A unique feature of oocytes is that centrosomes are eliminated during oogenesis in many animals (Szollosi et al, 1972; McKim and Hawley, 1995; Holubcovaet al., 2015)
We found that the late equator accumulation of MKlp1/Pavarotti is regulated by a mechanism distinct from that in mitosis
We hypothesized that the composition or distribution of microtubule regulators within the bipolar spindle changes to confer extra spindle stability during the arrest
Summary
A unique feature of oocytes is that centrosomes are eliminated during oogenesis in many animals (Szollosi et al, 1972; McKim and Hawley, 1995; Holubcovaet al., 2015). We hypothesized that localization changes of crucial microtubule regulators may stabilize the bipolar spindle during the long prometaphase I or metaphase arrest in oocytes. Two microtubule cross-linking kinesins, MKlp1/Pavarotti (Pav) and kinesin-5/Klp61F, accumulate in the spindle equator only later during the metaphase I arrest.
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